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Morphology, Behaviour and Molecular Evolution of Giant Mouse Lemurs (Mirza Spp.) Gray, 1870, with Description of a New Species

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Morphology, Behaviour and Molecular Evolution of Giant Mouse Lemurs (Mirza Spp.) Gray, 1870, with Description of a New Species P.M. Kappeler et al.: A New Mirza Species MORPHOLOGY, BEHAVIOUR AND MOLECULAR EVOLUTION OF GIANT MOUSE LEMURS (MIRZA SPP.) GRAY, 1870, WITH DESCRIPTION OF A NEW SPECIES. Kappeler PM, Rasoloarison RM, Razafimanantsoa L, Walter L and Roos C Key Words: Mirza, morphometrics, biogeography, phylogeny, mitochondrial cyto- chrome b, Microcebus, new species Abstract Giant mouse lemurs (genus Mirza) are small nocturnal primates endemic to Madagascar, of which a single species (M. coquereli) is currently recognized. It is dis- tributed along Madagascar’s west coast, with a gap of several hundred kilometres between two presumed subpopulations. Previous studies in the field and in captivity indicated substantial differences in several aspects of the biology of these two subpopulations. We therefore collected morphometric, genetic and behavioural data from populations representing the southern and northern end of their range to ex- amine these differences in more detail. We obtained standard morphometric field measurements and DNA samples from a total of 74 adult males and females at Kirindy (central western Madagascar) and Ambato (northwestern Madagascar) and compared their social organisation. We also studied a total of 9 Mirza specimens housed at the Rijksmuseum van Natuurlijke Historie Leiden (The Netherlands). Our morphometric analyses revealed that the two Mirza populations differed signif- icantly in 12 out of 13 measures, with the northern Mirza sporting smaller values in all traits except testes volume. Northern Mirza spent the day in nests with 2-8 (mean 4.1) individuals, whereas Mirza in the south virtually always slept alone. Moreover, reproduction in the northern population occurred several months earlier than in the south. We also sequenced the complete mitochondrial cytochrome b (cyt b) gene from several specimens and found that (1) the two populations differed by 3.33-3.51 %, which is similar to genetic distances observed among several closely re- lated species of mouse lemurs (Microcebus), (2) DNA extracted from tissue on skulls collected in 1868/1870 yielded partial cyt b sequences that aligned perfectly with the northern and southern population samples, respectively, and (3) Microcebus from Andasibe clearly differed genetically from all other known mouse lemur species, in- dicating a separate species status for this population. Based on the combination of morphological, behavioural and genetic differences between Mirza from Kirindy and Ambato we conclude that they should be separated at the species level. Because M. coquereli was described based on a specimen from the southern population, we de- scribe the northern Mirza as a species new to science. Introduction Madagascar is a global hot spot for biodiversity and conservation (GOODMAN and BENSTEAD, 2003; MITTERMEIER et al., 1998; MYERS et al., 2000; SECH- Primate Report 71, July 2005 3 P.M. Kappeler et al.: A New Mirza Species REST et al., 2002; YODER et al., 2005). Because of the number of endemic taxa and their phylogenetic history and position, the primates of Madagascar (Lemurifor- mes), in particular, represent one of the top global primate conservation priorities (GANZHORN et al., 1997a,b; JERNWALL and WRIGHT, 1998). Information about the taxonomic status, geographical distribution and abundance of individual taxa constitute the necessary scientific basis for the development of effective conserva- tion action plans and their legal implementation. In the case of lemurs, these basic data are still far from complete because many new taxa or new localities for known taxa continue to be described, even in the new millennium (GROVES, 2000; LOUIS et al., 2005; MAYOR et al., 2004; RASOLOARISON et al., 2000; THALMANN and GEISSMANN, 2002) and their phylogenetic relationships are far from being re- solved (FAUSSER et al., 2004; NIEVERGELT et al., 2002; PASTORINI et al., 2001a,b, 2002a,b, 2003; ROOS et al., 2004; YODER et al., 2000). Ongoing field stud- ies, genetic analyses and museum work all indicate that the full taxonomic diversity of lemurs is still incompletely described and that conservation priorities need to be updated constantly. The mouse and dwarf lemurs (Cheirogaleidae) represent the largest lemur fam- ily. All members of the five currently recognized genera (Allocebus, Cheirogaleus, Microcebus, Mirza and Phaner) are relatively small (< 500 g) and nocturnal (MAR- TIN, 1972). Several field studies of cheirogaleids initiated in the 1990s used exten- sive trapping, detailed morphometrics and various genetic tools to address questions about their behavioural ecology. These new kinds of data also revealed the existence of new species (SCHMID and KAPPELER, 1994; ZIMMERMANN et al., 1998) and prompted systematic taxonomic work on this group, using a combination of osteo- logical, morphometrical and genetic data (GROVES, 2000; PASTORINI et al., 2001b; RASOLOARISON et al., 2000; RUMPLER et al., 1998; YODER et al., 1996, 2000, 2002). Despite difficulties arising from many synonyms, missing and damaged holotypes or those with vague collection localities and descriptions based on lecto- types or neotypes, the previously single recognized species of west coast mouse le- mur (Microcebus murinus) could be differentiated into seven different species, three of which were new to science (RASOLOARISON et al., 2000). A similar taxonomic revision of the genus Cheirogaleus, albeit based on analyses of museum specimens alone, has indicated the existence of several species of dwarf lemurs along Madagas- car’s east coast, where traditionally only one species (C. major) had been recognized (GROVES, 2000). The overdue re-evaluations of the taxonomic status and phylogen- etic position of Phaner and Allocebus still await further field data (GROVES and TATTERSALL, 1991). The genus Mirza GRAY, 1870 is currently represented by a single recognized spe- cies: Coquerel's dwarf lemur, M. coquereli (GRANDIDIER, 1867). While mainly con- sidered as a mouse lemur (e.g. PETTER and PETTER-ROUSSEAUX, 1979), it was resurrected as separate genus by TATTERSALL (1982) because of its larger size and various behavioural and morphological differences with Microcebus. The genus Mir- za is restricted to western lowland forests, where it appears to have a disjunct distri- bution, with a gap between subpopulations spanning several hundred kilometres (Fig. 1). However, neither the exact limits of remaining population centres, nor the actual and historical presence or absence of Mirza in the intermediate regions are known (MITTERMEIER et al., 1994; PETTER et al., 1977; TATTERSALL, 1982). 4 Primate Report 71, July 2005 P.M. Kappeler et al.: A New Mirza Species Today, Mirza is found in the Sambirano region, with the northern Mahavavy river as a possible northern boundary of this species’ range, whereas in the south, it is known to occur between the Parc National de Bemaraha and the Parc National de Zombitse-Vohi- basia, with a possible sou- thern limit of their distri- bution somewhere north of the Onilahy river (KAPPE- LER, 2003). Most recently, Mirza has also been sighted in the Réserve Naturelle Intégrale Tsingy de Namo- roka (S. GOODMAN, pers. comm.), which is between these two distribution nu- clei. The behavioural ecology of Mirza has been studied both near the southern and northern ends of its geogra- phical distribution. The first detailed description of the natural history of Mir- za was provided by PET- TER et al. (1971), who col- lected opportunistic obser- vations near Beroboka, Fig. 1: Distribution of the genus Mirza (black: confir- north of Morondava. AN- med, grey: inferred). Dots indicate origin of analysed DRIANARIVO (1981) con- Mirza and Microcebus samples (see also Table 1). ducted the first systematic study of ranging and social behaviour in the northern population on the Ampasindava Peninsula near Am- pasikely, northwest of Ambanja. A study by PAGES (1978, 1980) in Marosalaza for- est north of Morondava focused on social organisation and feeding ecology. Finally, an ongoing study in Kirindy Forest (CFPF) north of Morondava has provided data on the social and genetic structure of another southern population (KAPPELER, 1997a; KAPPELER et al., 2002). The largest captive population of Mirza, which is housed at Duke University Primate Centre, was the subject of several behavioural and physio- logical studies (STANGER, 1995; STANGER et al., 1995). This colony was estab- lished in 1982 with animals from the Ambanja region captured near Antamboro be- tween the villages of Ampasimbary and Ampasindava (D. HARING, pers. comm.). Primate Report 71, July 2005 5 P.M. Kappeler et al.: A New Mirza Species These previous studies have indicated the possible existence of behavioural and morphological differences between the northern and southern populations, e.g. in sexual dimorphism, relative testes size and seasonality of reproduction (KAPPE- LER, 1997a,b, 2003; but see ALBRECHT et al., 1990), but a direct comparison has not been attempted. To investigate possible taxonomic differentiation that may un- derlie these differences, we initiated a comparative field study of the northern and southern population and examined museum specimens from both regions. We con- clude that the observed behavioural, morphological and genetic differences merit separation of the two populations at the species level and describe the northern pop- ulation of Mirza as a new species. Materials and Methods Fieldwork Field studies of Mirza were conducted in Kirindy Forest (20°40'S, 44°39'E), where the German Primate Centre maintains a permanent research station, and on the Ambato Peninsula, situated between the town of Ambanja and the island of Nosy Faly, where we found Mirza at the same site on Ermitage beach (13°25'S, 48°29'E) where ANDRIANARIVO (1981) conducted his study. At Kirindy, Mirza has been studied continuously since 1993, whereas we studied the Ambato population during three separate trips in March 1999, April 2000 and October 2000. The study area in the dry deciduous forest at Kirindy has been described in great detail elsewhere (KAPPELER, 1997a; SORG et al., 2003). At Ambato, Mirza was found in a highly de- graded 4 ha patch of forest at the tip of a small peninsula next to the Hotel Ermitage Plage.
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